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A genomic snapshot of demographic and cultural dynamism in Upper Mesopotamia during the Neolithic Transition
Abstract
Upper Mesopotamia played a key role in the Neolithic Transition in Southwest Asia through marked innovations in symbolism, technology, and diet. We present 13 ancient genomes (c. 8500 to 7500 cal BCE) from Pre-Pottery Neolithic Çayönü in the Tigris basin together with bioarchaeological and material culture data. Our findings reveal that Çayönü was a genetically diverse population, carrying mixed ancestry from western and eastern Fertile Crescent, and that the community received immigrants. Our results further suggest that the community was organized along biological family lines. We document bodily interventions such as head shaping and cauterization among the individuals examined, reflecting Çayönü’s cultural ingenuity. Last, we identify Upper Mesopotamia as the likely source of eastern gene flow into Neolithic Anatolia, in line with material culture evidence. We hypothesize that Upper Mesopotamia’s cultural dynamism during the Neolithic Transition was the product not only of its fertile lands but also of its interregional demographic connections.
https://www.science.org/doi/10.1126/sciadv.abo3609#.Y2VYXzoOlFM.twitter
Abstract
Upper Mesopotamia played a key role in the Neolithic Transition in Southwest Asia through marked innovations in symbolism, technology, and diet. We present 13 ancient genomes (c. 8500 to 7500 cal BCE) from Pre-Pottery Neolithic Çayönü in the Tigris basin together with bioarchaeological and material culture data. Our findings reveal that Çayönü was a genetically diverse population, carrying mixed ancestry from western and eastern Fertile Crescent, and that the community received immigrants. Our results further suggest that the community was organized along biological family lines. We document bodily interventions such as head shaping and cauterization among the individuals examined, reflecting Çayönü’s cultural ingenuity. Last, we identify Upper Mesopotamia as the likely source of eastern gene flow into Neolithic Anatolia, in line with material culture evidence. We hypothesize that Upper Mesopotamia’s cultural dynamism during the Neolithic Transition was the product not only of its fertile lands but also of its interregional demographic connections.
RESULTS AND DISCUSSION
We studied the skeletal remains of 33 individuals from Çayönü (Fig. 1, A and B, and table S3). These were mainly found as subfloor burials located inside or within the proximity of six Pre-Pottery Neolithic B (PPNB) buildings (table S1). We screened 33 aDNA libraries by shotgun sequencing, which revealed endogenous DNA proportions varying between 0.04 and 5% (median = 0.2%; fig. S1). This was lower than aDNA preservation in a contemporaneous Central Anatolian settlement, Aşıklı (median = 1.4%, Wilcoxon rank sum test, P < 0.05), but comparable to another Central Anatolian site of a similar date, Boncuklu (median = 0.1%, Wilcoxon rank sum test, P > 0.05; fig. S2).
Libraries from 14 individuals were chosen for deeper sequencing (Materials and Methods), from which we generated shotgun genomes with depths ranging from 0.016× to 0.49×. (fig. S1 and table S3). High rates of postmortem damage accumulation at read ends, short average fragment sizes [49 to 60 base pairs (bp), median = 51.4 bp], and mitochondrial haplotype-based estimates suggested the authenticity of all 14 libraries (Materials and Methods) (table S3). With these data, we first estimated genetic kinship among all individual pairs (Materials and Methods). Two samples, both identified as female infants (cay018 and cay020), were genetically inferred either to belong to the same individual or to be identical twins. Skeletal analyses also suggested that both petrous bones could belong to the same individual. We therefore merged their genomic data and treated these merged data as representing a single individual, reducing our sample size to 13 (6 adult females, 2 adult males, 3 subadult females, and 2 subadult males). We further identified four related pairs of first to third degree (see below) and removed all but one individual among sets of closely related individuals in population genetic analyses (Materials and Methods).
The east-west genetic structure of Neolithic Southwest Asia
To obtain an overview of genetic affinities among human populations in Neolithic Southwest Asia, we compared the 13 Çayönü genomes with published ancient genomes dating to c. 15,000 to 5500 BCE from the Fertile Crescent and neighboring regions (table S4) (7–9, 12, 13, 22–25) using multidimensional scaling (MDS) of pairwise f3 results, D-statistics, and qpAdm analyses (26). These led to a number of observations. In the MDS analysis, the Çayönü group occupied a distinct and intermediate position within the space of Southwest Asian genetic diversity bordered by early Holocene South Levant, Central Zagros and South Caucasus, and Central Anatolia (Fig. 1D and fig. S3). Our sample of Çayönü genomes was internally homogeneous within this space, with the exception of an “outlier” individual, cay008, who appeared relatively closer to Zagros/Caucasus individuals. D-statistics likewise showed that the Çayönü group was genetically closer to western Southwest Asia, and particularly to early Holocene Central Anatolia, than to eastern Southwest Asia (Central Zagros) (Fig. 2A and table S5). At the same time, Central Zagros genomes showed higher genetic affinity to our Çayönü sample than to Central Anatolia or South Levant (Fig. 2B). Last, we found that cay008 harbors higher Zagros contribution than other Çayönü individuals (Figs. 1D and 2C, figs. S4 to S6, and table S6)..........
An early Neolithic demographic shift in the “Fertile Crescent”
Our dataset further allowed us to revisit a previous observation on the demographic impact of the Neolithic Transition. It had been earlier reported that the Central Anatolian PPN populations Aşıklı and Boncuklu had low levels of genetic diversity, similar to Upper Paleolithic and Mesolithic Europeans and Caucasians (9, 13). In comparison, Central Anatolian PN populations Tepecik-Çiftlik and Çatalhöyük, as well as West Anatolian and European Neolithic populations, carried higher genetic diversity levels. This temporal increase in genetic diversity was attributed to the transition to farming and associated intensification of population movements and admixture [(9); also see (12)].
Here, we asked whether PPN populations in the Fertile Crescent, which comprises the main domestication centers of animals and plants in Southwest Asia, also had low genetic diversity levels similar to the Central Anatolian PPN groups. Measuring genetic diversity using outgroup f3 values in genetic samples from Upper Mesopotamia (Çayönü), South Levant (Ain Ghazal), and Central Zagros (Ganj Dareh), we found that genetic samples from all three Fertile Crescent PPN settlements had higher diversity levels than those of the Central Anatolia PPN and are on a par with those of later-coming PN communities of Central and Western Anatolia (Fig. 5A and table S7). We note, however, that this relatively high within-population diversity does not seem to involve visible interindividual differences in ancestry proportions (e.g., variable Zagros ancestry) within the Çayönü sample but may be attributed to heterozygosity within the group (figs. S5 to S7 and note S4)....
https://www.science.org/doi/10.1126/sciadv.abo3609#.Y2VYXzoOlFM.twitter